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Abstract

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Portal vein thrombosis (PVT) occurs in ≤12% of pediatric recipients of liver transplantation (LT). Known complications of PVT include portal hypertension, allograft loss, and mortality. The management of PVT is varied. A single-center, case-control study of pediatric LT recipients with portal vein (PV) changes after LT was performed. Cases were categorized as early PVT (if PVT was detected within 30 days of transplantation) or late PVT (if PVT was detected more than 30 days after transplantation or if early PVT persisted beyond 30 days). Two non-PVT control patients were matched on the basis of the recipient weight, transplant indication, and allograft type to each patient with PVT. Thirty-two of the 415 LT recipients (7.7%) received 37 allografts and developed PVT. In comparison with control patients, a higher proportion of patients with PVT had PVT present before LT (13.3% versus 0%, P = 0.01). Patients with early PVT usually returned to the operating room, and 9 of 15 patients (60%) had PV flow restored. Patients with late PVT had lower white blood cell (4.9 [1000/μL] versus 6.8 [1000/μL], P < 0.01) and platelet counts (140 [1000/μL] versus 259 [1000/μL], P < 0.01), an elevated international normalized ratio (1.2 versus 1.0, P < 0.001), and more gastrointestinal bleeding (25% versus 8.3%, P = 0.03) compared to controls. Patients with PVT were also less frequently at the expected grade level (52% versus 88%, P < 0.001). The patient survival rates were 84%, 78%, and 78% and 91%, 84%, and 79% for cases and controls at 1, 5, and 10 years, respectively. The allograft survival rates were 90%, 80%, and 80% for cases and 94%, 89%, and 87% for controls at 1, 5, and 10 years, respectively. In conclusion, patients with early and late PVT had preserved allograft function, and there was no impact on mortality. Patients diagnosed with early PVT often underwent operative interventions with successful restoration of flow. Patients diagnosed with late PVT experienced variceal bleeding, and some required portosystemic shunting procedures. Academic delays were also more common. In late PVT, the clinical presentation dictates care because the optimal management algorithm has not yet been determined. Multi-institutional studies are needed to confirm these findings and improve patient outcomes. Liver Transpl 19:315–321, 2013. © 2013 AASLD.

Abbreviations
CT

computed tomography

INR

international normalized ratio

LT

liver transplantation

MR

magnetic resonance

MSOF

multisystem organ failure

NS

not significant

PTP

percutaneous transhepatic portography

PV

portal vein

PVS

portal vein stenosis

PVT

portal vein thrombosis

Liver transplantation (LT) is the standard treatment for end-stage liver disease in children. As the surgical and medical care of transplant patients has improved, so has long-term survival, with expected survival beyond 5 years at greater than 80% in the pediatric population.[1] With improved survival, the management of morbidity and its impact on long-term outcomes have become paramount. Portal vein (PV) obstructions caused by portal vein thrombosis (PVT) or portal vein stenosis (PVS) after LT occur in up to 12% of recipients and most often occur immediately after LT.[2, 3] When PVT occurs soon after transplantation (early PVT), urgent management may be necessary and require a return to the operating room for PV thrombectomy or the placement of interposition grafts because allograft survival and potentially patient survival may be negatively affected without restoration of PV flow.

When PVT occurs at a later time (late PVT) or if early PVT cannot be resolved but allograft function is maintained, the clinical implications vary and range from an asymptomatic patient diagnosed by ultrasound to a patient with manifestations of portal hypertension such as an enlarging spleen, a declining platelet count, and gastrointestinal bleeding from varices. Because mesenteric blood is diverted around the liver, it is possible for patients to develop subtle neuropsychiatric changes that result in decreased cognitive skills. The management of late PVT is less well defined because minimally affected allograft function is typical, and a conservative, observational approach may be considered, with endoscopic variceal ligation or surgical portosystemic shunts reserved for patients who develop episodes of gastrointestinal bleeding.

There are limited data describing the natural history of early and late PVT. Furthermore, the ideal management of PVT beyond the immediate posttransplant period has not been defined, with only small case series to guide medical decision making. Accordingly, we reviewed our transplant center's experience with the aims of identifying the rates of both early and late PVT, the risk factors associated with PVT development, and the frequency of complications in patients with PVT and describing our management of late PVT with associated outcomes.

PATIENTS AND METHODS

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

This study was approved by the institutional research review board of Cincinnati Children's Hospital Medical Center (Cincinnati, OH). A single-center, case-control study of pediatric patients with PVT after LT was performed. Cases were identified by a review of the LT database from July 1986 through August 2010; diagnostic codes for PVT and PVS were used to identify all patients with PV changes requiring an intervention or further evaluation. Two transplant recipients without PV changes were matched to each case on the basis of the weight at the time of transplantation, the PV anastomotic technique (interposition or end-to-end), the allograft type (whole or reduced with reduced allografts matched for split or size reduced grafts as able), the operative time of the transplant, and the pretransplant diagnosis. Patients whose transplant was not performed at the center were excluded from the study.

All LT recipients were evaluated with daily Doppler ultrasound imaging for the first 5 days after the operation. Subsequent ultrasound examinations were performed when they were warranted (usually for changes in clinical or biochemical parameters). Additionally, an ultrasound examination was performed at each annual follow-up visit. Abnormal ultrasound findings led to further imaging with computed tomography (CT), magnetic resonance (MR) imaging, or transhepatic portal venography.

Early PVT was defined as PVT detected within 30 days of LT. Late PVT was defined as PVT detected more than 30 days after LT or as early PVT persisting after 30 days.

Demographic, radiographic, endoscopic, and long-term data were abstracted from medical records with outcome data collected prospectively from annual transplant forms obtained at each follow-up visit. Long-term data were obtained from surviving patients whose care had not been transferred.

Statistical Methods

Differences between patients with PVT and patients without PVT were evaluated with Fisher's exact test and the Kruskal-Wallis test as appropriate, with differences between groups evaluated with an analysis of variance. A survival analysis was performed for all patients, and P < 0.05 was used throughout the analysis; 95% confidence intervals were calculated. SAS 9.2 (SAS Institute, Cary, NC) was used for group comparisons, and GraphPad Prism 5.0 (GraphPad Software, Inc., La Jolla, CA) was used for survival analysis.

RESULTS

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Study Population

From 1986 to August 2010, 415 patients underwent 468 LT procedures. Population characteristics are presented in Table 1. Forty-one patients (9.9%) who had PV changes on ultrasound that required confirmatory studies or interventions were identified (Fig. 1). PVT was confirmed in 32 patients (7.7%), and 19 cases were detected during the first 30 days. Isolated PVS occurred in 5 (1.2%). The remaining 4 patients had concerning ultrasound examinations 0 to 11 days after LT, but PVT was excluded by an intraoperative evaluation (n = 3) or a CT angiogram (n = 1).

image

Figure 1. Flowchart of patients with PVT and outcomes. *The surgical interventions were interposition grafts (n = 5) and thrombectomy/revision (n = 11). †The retransplant indications were hepatic artery thrombosis with graft failure (n = 2) and chronic rejection (n = 1). ‡The causes of death were allograft failure associated with vascular thrombosis (n = 2), cardiac arrest (n = 1), and complications of congenital heart disease (n = 1). §The retransplant indication was recurrent autoimmune hepatitis (n = 1). ∥The causes of death were MSOF with the recurrence of Langerhans cell histiocytosis (n = 1), sepsis associated with bowel necrosis (n = 1), and MSOF (n = 1). ¶The shunt types were H-type mesocaval shunts (n = 4) and a revision to a distal splenorenal shunt (n = 1). #The cause of death was MSOF (n = 1).

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Table 1. Demographics of Patients With PVT and Controls
CharacteristicPatients With PVT (n = 32)Controls (n = 82)P Value
  1. a

    The patients were matched on these characteristics.

  2. b

    The data are expressed as medians and ranges.

Recipients   
Male [n (%)]14 (44)40 (49)NS
Biliary atresia [n (%)]a20 (63)51 (62)NS
Age (years)b1.0 (0.5–9.8)1.2 (0.1–12.8)NS
Weight (kg)ab8.1 (4.1–38.9)8.5 (2.5–38.8)NS
PVT before LT [n (%)]4 (12.5)0 (0)0.01
Preduodenal PV [n (%)]2 (6.3)4 (4.9)NS
Donors   
Whole organ [n (%)]a14 (44)36 (44)NS
Interposition graft [n (%)]a3 (9.4)2 (2.4)NS
Deceased donor [n (%)]28 (88)77 (94)NS
Donor/recipient weight ratiob2.3 (0.8–12.3)2.2 (0.6–13.7)NS

Indications for Transplantation and Risk Factors for PVT

Biliary atresia was the most common indication for transplantation in both the case and control cohorts. A higher proportion of patients with PVT after LT had PVT present before transplantation in comparison with the controls (13.3% versus 0%, P = 0.01). No other recipient or donor variable was associated with developing PVT (Table 1).

A thrombophilia workup was performed for only 5 patients in this study population (3 patients with PVT and 2 control patients). The workup for both control patients occurred after transplantation for access site thrombosis, whereas delayed workup for the patients with PVT occurred when there was concern about shunt patency after placement. All of these patients had mildly abnormal findings. Among the patients with PVT, one patient had low protein C, protein S, and antithrombin III levels; another had mildly decreased protein S levels; and the third patient had a slightly increased plasminogen activator inhibitor 1 level. The abnormal findings for the 2 control patients were positivity for lupus anticoagulant antibodies in one and low protein C levels in the other. None of the patients were treated.

Early PVT: Diagnosis, Management, and Outcomes

Eighteen of the 19 patients (95%) with early PVT (detected within 30 days of transplantation) were identified within the first 4 days after LT. One patient was diagnosed on postoperative day 15. Operative interventions were performed for 16 patients; thrombectomy (n = 7), thrombectomy with interposition graft placement (n = 3), interposition graft placement (n = 2), anastomotic revision (n = 1), or some other combination (n = 3) was performed. The other 3 patients were followed clinically because they were asymptomatic with normal allograft function. In 2 of these patients, subsequent imaging confirmed PVT with cavernous transformation, 1 patient had absent flow, and 1 of the 3 patients underwent endoscopy demonstrating varices.

Allograft failure requiring retransplantation occurred in 3 of the 19 patients (15.8%) 3, 49, and 245 days after primary LT (the first 2 retransplants were performed for concurrent hepatic artery thrombosis, and the third was for chronic rejection). All 3 patients had undergone reoperation for PVT within the first 48 hours after the initial LT procedure. Four patients with early PVT died 3, 4, 73, and 339 days after transplantation. The deaths at 3 and 4 days were due to allograft failure associated with vascular thrombosis, and the late deaths were due to cardiac arrest and complications of congenital heart disease.

Long-term PV patency was achieved in 9 of the 15 survivors. For the 15 survivors, long-term follow-up was available for a median of 10.8 years (range = 4.0–19.2 years). All had good allograft function (see Table 2).

Table 2. Biochemical Profiles of Surviving Patients Whose Care Had Not Been Transferred at the Most Recent Follow-Up
VariablePatients With Early PVT (n = 9)Patients With Late PVT (n = 15)Controls (n = 54)P Value
  1. NOTE: The data are expressed as medians and interquartile ranges.

  2. a

    All 3 groups were significantly different.

  3. b

    Patients with late PVT significantly differed from both patients with early PVT and controls.

  4. c

    Patients with late PVT differed from controls.

Follow-up (years)10.8 (9.1–17.8)9.0 (4.2–12.7)7.3 (5.0–10.2)NS
Total protein (g/dL)7.9 (7.5–8.1)6.8 (6.4–7.1)7.6 (7.1–7.9)<0.0001a
Albumin (g/dL)4.5 (4.3–4.6)4.1 (3.7–4.2)4.3 (4.0–4.5)0.002b
Conjugated bilirubin (mg/dL)0 (0–0)0 (0–0)0 (0–0)NS
Alanine aminotransferase (U/L)35 (21–59)32 (15–44)26 (16–41)NS
Aspartate aminotransferase (U/L)47 (44–71)54 (45–66)51 (37–69)NS
White blood cells (1000/μL)6.3 (5.5–8.3)3.3 (2.4–5.1)6.8 (5.1–8.5)0.005b
Hemoglobin (g/dL)14.1 (13.6–14.6)12.8 (12.1–13.6)13.7 (12.6–14.3)NS
Platelets (1000/μL)228 (141–328)104 (69–156)259 (196–294)<0.001b
INR1.0 (1.0–1.1)1.2 (1.1–1.4)1.1 (1.0–1.1)0.0002c

Late PVT: Diagnosis, Management, and Outcomes

Late PVT was detected in 13 patients (3.1%) at a median of 3.3 years (range = 80 days to 15 years) after transplantation. To evaluate the impact of chronic PVT, we grouped these 13 patients with the 6 surviving patients with early PVT in whom PV patency could not be restored, and this resulted in a 19-patient cohort.

Ultrasound was the imaging modality used to identify PV changes in all 19 patients. Fifteen had subsequent imaging, which included CT angiography (n = 6), MR angiography (n = 6), and interventional angiography (n = 3). Additional imaging was not pursued in 4 patients because 2 died (described later) and 2 were asymptomatic. One of these had cavernous transformation at the time of diagnosis; the other had flow reversal.

Allograft failure requiring retransplantation occurred in 2 patients. In the first patient, PVT was diagnosed 3.5 years after the initial LT procedure, and retransplantation for recurrent autoimmune hepatitis occurred 1.2 years after late PVT was identified. In the second patient, PVT was found 80 days after retransplantation for chronic rejection, and the patient succumbed 82 days later because of multisystem organ failure (MSOF).

Three other patients with late PVT also expired 1.0, 1.4, and 17.5 years after LT because of intestinal ischemia and MSOF of an uncertain etiology, recurrence of Langerhans cell histiocytosis, and MSOF after a portosystemic shunt operation for gastrointestinal bleeding, respectively.

Long-Term Outcomes and Morbidity Associated With PVT

At the most recent follow-up, surviving patients with PVT had intact liver function as evidenced by normal albumin and conjugated bilirubin levels. In the late-PVT cohort, the white blood cell and platelet counts were lower, and this was attributable to hypersplenism (Table 2). The measured international normalized ratio (INR) was mildly elevated in the group with late PVT (1.2 versus 1.0 for patients with early PVT and 1.1 for controls, P < 0.001), but the clinical significance of this finding is uncertain.

Gastrointestinal bleeding occurred in 7 of 19 patients (37%) with late PVT and in 1 of 13 patients (7.7%) with early PVT, presumably from varices within the Roux limb. Nonvariceal gastrointestinal bleeding occurred in 7 of 82 controls (8.5%, P = 0.03). Endoscopy was performed only when gastrointestinal bleeding occurred or when it was clinically indicated. Six of the 7 patients with late PVT who underwent upper endoscopy (85.7%) had varices identified, with variceal ligation performed as indicated. Varices were identified within the Roux limb in 4 of these 7 patients, and because of persistent gastrointestinal bleeding, these patients underwent mesocaval shunt creation. The bleeding began a median of 4.9 years (range = 1.5–17 years) after transplantation. Bleeding that required transfusions occurred in 11 of 15 episodes; this included 1 patient who required >10 U during a stay in the intensive care unit. Each patient underwent 2 to 4 endoscopy procedures during his or her evaluation. Endoscopy, additional imaging [eg, formal angiography (n = 1) and MR angiography (n = 4)], or both revealed varices in the Roux limb, but only 2 of the 4 patients had esophageal varices amenable to variceal ligation, and with persistent symptoms, a surgical intervention was performed. Meso-Rex shunts were considered in all 4 patients; however, technical challenges, including hilar varices, dense bowel adhesions, and the allograft type (living donor left lateral segment), precluded access to the residual Rex recess. Mesocaval H-type shunts from the superior mesenteric vein to the inferior vena cava with ring Gore-Tex grafts were performed. Three patients responded without further bleeding episodes. For 1 patient, the procedure failed, and central splenorenal shunt creation was required 7 months later.

With respect to the functional status of the patients, no differences existed between cases and controls in physical function. An analysis of academic performance, however, demonstrated that only 52% of cases versus 88% of controls were enrolled at their expected grade level (odds ratio = 0.14, 95% confidence interval = 0.05–0.4, P = 0.0001). This association is likely multifactorial and difficult to interpret because the average age at transplantation for these patients was 2.6 years.

Overall Allograft and Patient Survival

Patient survival was not statistically different between cases (84%, 78%, 78%, and 78% at 1, 3, 5, and 10 years, respectively) and controls (91%, 85%, 84%, and 79% at 1, 3, 5, and 10 years, respectively). Allograft survival was also similar with rates of 90%, 90%, 80%, and 80% for patients with PVT and rates of 94%, 89%, 89%, and 87% for controls at 1, 3, 5, and 10 years, respectively.

DISCUSSION

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

The incidence of PVT in our series is similar to that described for other transplant centers.[4, 5] Risk factors associated with PVT vary, but in our series, only the presence of pretransplant PVT was associated with developing PVT after LT. This has also been reported in adult studies.[6] Other studies have shown that children with biliary atresia are at increased risk for developing PV complications, with the PV size, the recipient age, and the recipient weight at the time of transplantation being significant predictors.[4, 7, 8] Adult studies have shown that interposition grafts, which were used in 9.4% of the primary LT procedures for our patients, are associated with PVT,[9] but this was not observed in our study.

It is unclear what role hypercoagulability played in the development of PVT because few of our patients underwent a prothrombotic evaluation. Protein C deficiency has been associated with PVT after LT and with PVT in non–LT-related pediatric cohorts.[10, 11] Additional research will be required to determine the impact of minor thrombophilic changes on the timing and development of PVT.

Morbidity was clearly increased in patients with PVT because gastrointestinal bleeding occurred in 25% of the PVT cases, and varices not amenable to endoscopic variceal ligation were frequently encountered. The frequency of varices, however, could be lower than this study has estimated because only pediatric patients with gastrointestinal bleeding or another indication would undergo invasive procedures, and this leads to an inherent screening bias.

A previously undescribed morbidity in our cohort was that patients with PVT were also less likely to be enrolled at grade level in comparison with their controls, although the etiology of this academic disparity is not known. Formal intelligence or psychomotor testing was not performed to identify an association between PVT, possible hepatic encephalopathy, and academic performance, and this limits any conclusions that can be drawn from this finding. Additionally, the majority of these children underwent transplantation before they entered grade school, and this limits our ability to assess the pretransplant status of this retrospective cohort. Pediatric LT recipients more commonly suffer cognitive delays and academic challenges than healthy controls, but the reason for this difference is unknown.[12] It is plausible that the academic delays reflect decreased school attendance due to the morbidity and hospitalizations associated with PVT. Alternatively, the decline in academic function may be related to minimal hepatic encephalopathy, which is seen in nearly one-third of pediatric patients with PV obstructions.[13]

Varied surgical interventions can be attempted for portal hypertension; in this series, meso-Rex bypass was considered, but technical limitations precluded safe exploration, and central shunts were used. Recent studies have demonstrated the effectiveness of meso-Rex bypass in restoring portal blood flow. In addition to improving flow, this may improve the cognitive abilities of patients and hematological parameters associated with hypersplenism.[14, 15] A recent review of published experiences with this technique showed excellent results with reported 100% long-term patency.[16] A meso-Rex shunt should be considered if it is feasible; however, a thorough understanding of shunt procedures must be available because all shunt types may need to be employed for this complex population.

Additionally, our patients who had late PVT had evidence of hypersplenism with thrombocytopenia. Although the median platelet count will typically be adequate for most minor procedures, this type of patient is at increased risk for variceal bleeding from associated portal hypertension and splenic rupture if he or she is involved in contact sports or trauma. Additionally, a patient with splenomegaly may have an impacted immune system, and this should be remembered for the immunosuppressed transplant recipient.[17] The mild elevation of INR seen in our patients with late PVT is also notable because it may reflect underlying coagulation abnormalities, as described previously in noncirrhotic portal hypertension.[18]

Even though morbidity was clearly increased in our population, PVT did not compromise overall allograft or patient survival. This differs from a recent analysis reporting that PVT negatively affects survival when it occurs in the first 30 days after transplantation.[19] Other single-center pediatric series, however, have also shown survival rates unaffected by PVT,[20] although a recent large combined adult and pediatric series demonstrated that PV complications did decrease patient survival.[21]

For patients who develop late PVT, the ideal management algorithm has not yet been determined. In the largest series of PV complications in pediatric LT, patients with suspected PV changes immediately underwent percutaneous transhepatic portography (PTP) with balloon dilation or urokinase infusion.[5] A high success rate (69%) was achieved, but the results were not stratified by PVS versus PVT. Importantly, a previous study by this group demonstrated that venoplasty was less effective in cases of obstruction/thrombosis versus stenosis, as others have also shown.[22] When PTP was unsuccessful or was required frequently, a surgical intervention was attempted. These 2 studies demonstrate the value of PTP in PVS, but further studies are warranted before this invasive approach is adopted for complete thrombosis.

The limitations of this study include its retrospective design and incomplete follow-up. The infrequency of PVT makes risk factors and differences between groups difficult to detect and increases the possibility of statistical errors.

Future research can reasonably address these limitations. The role of clotting disorders and thrombophilic tendencies in developing PVT should be determined because this would enable potential preventive strategies, monitoring, and intervention. Additionally, an evaluation of the cognitive impact of PVT should be performed. The management of late PVT should also be evaluated to delineate the role and timing of angiography, medical therapy, endoscopic variceal ligation, and optimal surgical management because morbidity is clearly increased in these patients.

REFERENCES

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES
  • 1
    2009 Annual Report of the US Organ Procurement and Transplantation Network and the Scientific Registry of Transplant Recipients: Transplant Data 1999-2008. http://www.srtr.org/annual_reports. Accessed November 2012.
  • 2
    Buell JF, Funaki B, Cronin DC, Yoshida A, Perlman MK, Lorenz J, et al. Long-term venous complications after full-size and segmental pediatric liver transplantation. Ann Surg 2002;236:658666.
  • 3
    Moon JI, Jung GO, Choi GS, Kim JM, Shin M, Kim EY, et al. Risk factors for portal vein complications after pediatric living donor liver transplantation with left-sided grafts. Transplant Proc 2010;42:871875.
  • 4
    Ou HY, Concejero AM, Huang TL, Chen TY, Tsang LL, Chen CL, et al. Portal vein thrombosis in biliary atresia patients after living donor liver transplantation. Surgery 2011;149:4047.
  • 5
    Ueda M, Oike F, Kasahara M, Ogura Y, Ogawa K, Haga H, et al. Portal vein complications in pediatric living donor liver transplantation using left-side grafts. Am J Transplant 2008;8:20972105.
  • 6
    Tao YF, Teng F, Wang ZX, Guo WY, Shi XM, Wang GH, et al. Liver transplant recipients with portal vein thrombosis: a single center retrospective study. Hepatobiliary Pancreat Dis Int 2009;8:3439.
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    Chardot C, Herrera JM, Debray D, Branchereau S, DeDreuzy O, Devictor D, et al. Portal vein complications after liver transplantation for biliary atresia. Liver Transpl Surg 1997;3:351358.
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    Takahashi Y, Nishimoto Y, Matsuura T, Hayashida M, Tajiri T, Soejima Y, et al. Surgical complications after living donor liver transplantation in patients with biliary atresia: a relatively high incidence of portal vein complications. Pediatr Surg Int 2009;25:745751.
  • 9
    Harper PL, Edgar PF, Luddington RJ, Seaman MJ, Carrell RW, Salt AT, et al. Protein C deficiency and portal thrombosis in liver transplantation in children. Lancet 1988;2:924927.
  • 10
    Pinto RB, Silveira TR, Rosling L, Bandinelli E. Thrombophilic disorders in children and adolescents with portal vein thrombosis [in Portuguese]. J Pediatr (Rio J) 2003;79:165172.
  • 11
    Sorensen LG, Neighbors K, Martz K, Zelko F, Bucuvalas JC, Alonso EM; for Studies of Pediatric Liver Transplantation (SPLIT) and Functional Outcomes Group (FOG). Cognitive and academic outcomes after pediatric liver transplantation: Functional Outcomes Group (FOG) results. Am J Transplant 2011;11:303311.
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    Yadav SK, Srivastava A, Srivastava A, Thomas MA, Agarwal J, Pandey CM, et al. Encephalopathy assessment in children with extra-hepatic portal vein obstruction with MR, psychometry and critical flicker frequency. J Hepatol 2010;52:348354.
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    Kishi Y, Sugawara Y, Matsui Y, Akamatsu N, Makuuchi M. Late onset portal vein thrombosis and its risk factors. Hepatogastroenterology 2008;55:10081009.
  • 14
    Mack CL, Zelko FA, Lokar J, Superina R, Alonso EM, Blei AT, Whitington PF. Surgically restoring portal blood flow to the liver in children with primary extrahepatic portal vein thrombosis improves fluid neurocognitive ability. Pediatrics 2006;117:e405e412.
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    Superina R, Bambini DA, Lokar J, Rigsby C, Whitington PF. Correction of extrahepatic portal vein thrombosis by the mesenteric to left portal vein bypass. Ann Surg 2006;243:515521.
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    de Ville de Goyet J, LoZupone C, Grimaldi C, D'Ambrosio G, Candusso M, Torre G, Monti L. Meso-Rex bypass as an alternative technique for portal vein reconstruction at or after liver transplantation in children: review and perspectives. Pediatr Transplant; doi:10.1111/j.1399-3046.2012.01784.x.
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    Li ZF, Zhang S, Lv GB, Huang Y, Zhang W, Ren S, et al. Changes in count and function of splenic lymphocytes from patients with portal hypertension. World J Gastroenterol 2008;14:23772382.
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    Raffa S, Reverter JC, Seijo S, Tassies D, Abraldes JG, Bosch J, García-Pagán JC. Hypercoagulability in patients with chronic noncirrhotic portal vein thrombosis. Clin Gastroenterol Hepatol 2012;10:7278.
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    Waits SA, Wojcik BM, Cai S, Mathur AK, Englesbe MJ. Portal vein thrombosis and outcomes for pediatric liver transplant candidates and recipients in the United States. Liver Transpl 2011;17:10661072.
  • 20
    Heffron TG, Pillen T, Smallwood G, Henry S, Sekar S, Casper K, et al. Incidence, impact, and treatment of portal and hepatic venous complications following pediatric liver transplantation: a single-center 12 year experience. Pediatr Transplant 2010;14:722729.
  • 21
    Duffy JP, Hong JC, Farmer DG, Ghobrial RM, Yersiz H, Hiatt JR, Busuttil RW. Vascular complications of orthotopic liver transplantation: experience in more than 4,200 patients. J Am Coll Surg 2009;208:896903.
  • 22
    Ueda M, Egawa H, Ogawa K, Uryuhara K, Fujimoto Y, Kasahara M, et al. Portal vein complications in the long-term course after pediatric living donor liver transplantation. Transplant Proc 2005;37:11381140.